Research Article |
Corresponding author: Domingo Lago-Barcia ( domingo.lagobarcia@gmail.com ) Academic editor: David Gibson
© 2021 Domingo Lago-Barcia, Marcos Santos Silva, Fernando Carbayo.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Lago-Barcia D, Silva MS, Carbayo F (2021) Revision and description of six species of Choeradoplana (Platyhelminthes, Tricladida), with an emendation to the genus. ZooKeys 1016: 1-48. https://doi.org/10.3897/zookeys.1016.59617
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Living representatives of the Neotropical genus Choeradoplana Graff, 1896 (Geoplaninae, Tricladida, Platyhelminthes) are easily recognized by the typical shape of the head which is laterally expanded, rolled-up, and ventrally provided with two glandular cushions. In this study, the morphology and phylogeny (cytochrome C oxidase subunit I gene) of several species of land planarians are taxonomically investigated. Four of the six species studied are new to science, namely: Ch. eudoxiae Silva & Carbayo, sp. nov., Ch. claudioi Lago-Barcia & Carbayo, sp. nov., Ch. onae Lago-Barcia & Carbayo, sp. nov., and Ch. riutortae Lago-Barcia & Carbayo, sp. nov. The species Choeradoplana albonigra and Ch. eudoxiae deviate from the usual body shape pattern in that the head does not present lateral expansions nor glandular cushions, becoming indistinguishable from its sister genus Cephaloflexa. Pseudogeoplana tristriata (Schultze & Müller, 1857) is also redescribed from a newly collected specimen and was discovered to be a member of Choeradoplana.
COI, flatworms, Geoplaninae, land planarians, rolled up, taxonomy
Members of the Neotropical land planarians genera Choeradoplana and Cephaloflexa (Platyhelminthes: Geoplanidae: Geoplaninae) can be easily ascribed to either genus based on the head shape, which is characteristically kept rolled up backwards in both genera. The two genera can be distinguished from each other in that the cephalic region in Choeradoplana is laterally expanded and ventrally provided with two glandular cushions separated by a longitudinal groove, whereas the cephalic region in Cephaloflexa is ventrally concave and the anterior third of the body becomes thinner very gradually.
In a recent multi-gene phylogenetic analysis of the Geoplaninae, representatives of a species preliminarily ascribed in the field to Cephaloflexa turned out to be nested in the Choeradoplana clade (
In this paper, we describe or redescribe six species of Brazilian land planarians of the genus Choeradoplana. The external aspect of two of these species is similar to that of Cephaloflexa, namely the above-mentioned C. albonigra, and a new species described herein. We also studied a greenish individual recently collected and identified it as Pseudogeoplana tristriata (Schultze & Müller, 1857). The remaining four species were also collected recently and are new to science. We sequenced a fragment of the cytochrome C oxidase subunit I gene (COI) of each specimen to infer the phylogenetic relationships of the species treated herein, and the other representatives of the genus available in the GenBank.
Each specimen was divided into two tissue portions, one for histology and one DNA extraction, respectively (see also section below ‘Morphological analysis’). Animal tissue destined for molecular studies was fixed in absolute ethanol and preserved at -20 °C. Genomic DNA was extracted using a standard ammonium acetate extraction protocol modified from
The phylogenetic analysis included the newly obtained partial nucleotide sequences for the COI gene (Table
All specimens included in this study (except for the holotype SMF No. 702, Ch. albonigra) (Table
The flatworms were examined and photographed in vivo before being killed with boiling water. Tissue portions destined for histology were fixed in 10% formaldehyde and preserved in 80% ethanol. Color descriptions of the body of living and preserved specimens follow the online palette RAL colors (RAL gemeinnützige GmbH, available at https://www.ral-farben.de/uebersicht-ral-classic-farben.html?&L=1). Body portions were progressively dehydrated in an ascending series of ethanol and cleared in clove oil. Eye distribution was assessed from specimens cleared in clove oil. Body portions were subsequently embedded in Paraplast Tissue Embedding Medium and the resulting blocks were sectioned at 5–7 μm intervals using a retracting rotary microtome. Ribbons of embedding medium were affixed with albumin-glycerol (1:1) on glass slides placed on a hot plate and stained with the method Mallory-Heidenhain as modified by
List of samples used in this study showing species name, field number, museum accession number, type specimen status, collection locality and date, and GenBank accession number.
Species | Field number | Accession number | Type specimen | Coll. locality in Brazil | Coll. date | GenBank acc. (COI) |
---|---|---|---|---|---|---|
Choeradoplana abaiba |
F3905 |
|
– | Parque Estadual da Serra do Tabuleiro, SC | 07/14/09 | MF802634 |
F3894 |
|
– | Parque Estadual da Serra do Tabuleiro, SC | 07/13/09 | MF802633 | |
F3865 |
|
– | Parque Estadual da Serra do Tabuleiro, SC | 07/12/09 | MF802631 | |
F3866 |
|
– | Parque Estadual da Serra do Tabuleiro, SC | 07/12/09 | MF802632 | |
F3864 |
|
Holotype | Parque Estadual da Serra do Tabuleiro, SC | 07/12/09 | MF802630 | |
F3312 |
|
Paratype | Parque Estadual da Serra do Tabuleiro, SC | 01/17/09 | MF802629 | |
F3270 |
|
– | Parque Estadual da Serra do Tabuleiro, SC | 01/15/09 | MF802628 | |
F3315 |
|
– | Parque Estadual da Serra do Tabuleiro, SC | 01/17/09 | HQ542891 | |
Choeradoplana agua |
F2214 |
|
– | Parque Estadual do Desengano, RJ | 03/19/08 | MF802637 |
F2205 |
|
Paratype | Parque Estadual do Desengano, RJ | 03/18/08 | MF802636 | |
F2204 |
|
Paratype | Parque Estadual do Desengano, RJ | 03/18/08 | MF802635 | |
F2205 |
|
Paratype | Parque Estadual do Desengano, RJ | 03/18/08 | KF971686 | |
F3952 |
|
Paratype | Parque Estadual do Desengano, RJ | 08/09/08 | KF971680 | |
Choeradoplana albonigra (Riester, 1938) |
|
– | Holotype | Teresópolis, RJ | 04/09/14 | – |
F2313 |
|
– | Reserva Biológica Augusto Ruschi, ES | 26/05/08 | KF971684 | |
F2391 |
|
– | Reserva Biológica Augusto Ruschi, ES | 27/05/08 | KF971683 | |
F3991 |
|
– | Parque Estadual do Desengano, RJ | 08/10/09 | – | |
F4024 |
|
– | Parque Estadual do Desengano, RJ | 08/11/09 | – | |
F4031 |
|
– | Parque Estadual do Desengano, RJ | 08/11/09 | – | |
F4081 |
|
– | Parque Estadual do Desengano, RJ | 08/13/09 | KC608327 | |
Choeradoplana banga Carbayo & Froehlich, 2012 | F3706 |
|
– | Parque Estadual da Cantareira, SP | 04/19/09 | MF802639 |
F3006 |
|
Paratype | Parque Estadual da Cantareira, SP | 12/14/08 | MF802638 | |
F2023 |
|
Holotype | Parque Estadual da Cantareira, SP | 01/30/08 | KC608267 | |
F3011 |
|
Paratype | Parque Estadual da Cantareira, SP | 12/14/08 | KC608301 | |
Choeradoplana benyai Lemos & Leal-Zanchet, 2014 | F3813 |
|
– | Parque Estadual da Serra do Tabuleiro, SC | 07/12/09 | MF802641 |
F3494 |
|
– | Floresta Nacional de São Francisco de Paula, RS | 01/28/09 | MF802640 | |
- | MZU PL.00151 | Paratype | Floresta Nacional de São Francisco de Paula, RS | 03/21/10 | KJ690049 | |
Choeradoplana sp. | F2332 |
|
– | Reserva Biológica Augusto Ruschi, ES | 26/05/08 | MW127841* |
F2390 |
|
– | Reserva Biológica Augusto Ruschi, ES | 27/05/08 | MW127842* | |
Choeradoplana bocaina Carbayo & Froehlich, 2012 | F2822 |
|
Holotype | Parque Nacional da Serra da Bocaina, SP | 09/08/09 | KC608288 |
F2104 |
|
Paratype | Parque Nacional da Serra da Bocaina, SP | 02/10/08 | KC608273 | |
F2803 |
|
Paratype | Parque Nacional da Serra da Bocaina, SP | 09/07/08 | KC608283 | |
Choeradoplana claudioi sp. nov. | F2424 |
|
Holotype | Reserva Biológica Augusto Ruschi, ES | 28/05/08 | MW127839* |
F2510 |
|
Paratype | Reserva Biológica Augusto Ruschi, ES | 29/05/08 | MW127840* | |
Choeradoplana eudoxiae Silva & Carbayo, sp. nov. | F3417 |
|
Holotype | Floresta Nacional de São Francisco de Paula, RS | 01/22/09 | – |
Choeradoplana gladismarie |
F3802 |
|
Paratype | Parque Estadual Intervales, SP | 07/07/09 | KC608326 |
F3092 |
|
Holotype | Parque Estadual Intervales, SP | 12/12/08 | KC608306 | |
Choeradoplana iheringi Graff, 1899 | F3465 |
|
– | Floresta Nacional de São Francisco de Paula, RS | 01/25/09 | MF802660 |
F3454 |
|
– | Floresta Nacional de São Francisco de Paula, RS | 01/25/09 | MF802658 | |
F3447 |
|
– | Floresta Nacional de São Francisco de Paula, RS | 01/25/09 | MF802654 | |
Choeradoplana iheringi Graff, 1899 | F3430 |
|
– | Floresta Nacional de São Francisco de Paula, RS | 01/23/09 | MF802651 |
F3409 |
|
– | Floresta Nacional de São Francisco de Paula, RS | 01/22/09 | MF802649 | |
- | MZU PL.00156 | – | ? | KJ690046 | ||
Choeradoplana marthae Froehlich, 1955 | F2137 |
|
– | Estação Biológica de Boraceia, SP | 02/14/08 | MF802665 |
Choeradoplana minima Lemos & Leal-Zanchet, 2014 | - | MZU PL.00143 | Paratype | Floresta Nacional de São Francisco de Paula, RS | 02/25/10 | KJ690052 |
- | MZU PL.00145 | Paratype | Floresta Nacional de São Francisco de Paula, RS | 06/09/11 | KJ690051 | |
Choeradoplana onae Lago-Barcia & Carbayo, sp. nov. | F2230 |
|
Paratype | Reserva Biologica de Ruschi, SP | 05/24/08 | MW127834* |
F2235 |
|
– | Reserva Biologica de Ruschi, SP | 05/24/08 | MW127837* | |
F2281 |
|
Paratype | Reserva Biologica de Ruschi, SP | 26/05/08 | MW127836* | |
F2310 |
|
Paratype | Reserva Biologica de Ruschi, SP | 26/05/08 | MW127838* | |
F2414 |
|
Holotype | Reserva Biologica de Ruschi, SP | 27/05/08 | MW127835* | |
F2311 |
|
– | Reserva Biologica de Ruschi, SP | 26/05/08 | KF971685 | |
Choeradoplana pucupucu |
F2844 |
|
Holotype | Parque Nacional da Serra da Bocaina, SP | 09/01/08 | MF802666 |
F2840 |
|
Paratype | Parque Nacional da Serra da Bocaina, SP | 09/20/08 | KC608293 | |
Choeradoplana riutortae Lago-Barcia & Carbayo, sp. nov. | F4217 |
|
Paratype | Parque Nacional da Serra dos Orgãos, RJ | 01/06/10 | MW148795 * |
F4218 |
|
Holotype | Parque Nacional da Serra dos Orgãos, RJ | 01/06/10 | – | |
F4261 |
|
Paratype | Parque Nacional da Serra dos Orgãos, RJ | 01/08/10 | – | |
Choeradoplana tristriata (Schultze & Müller, 1857) | F3226 |
|
– | Parque Estadual da Serra do Tabuleiro, SC | 01/11/09 | MW127833* |
Matuxia matuta (Froehlich, 1955) | F2184 |
|
– | Parque Estadual do Desengano, RJ | 03/17/08 | KC608276 |
F2187 |
|
– | Parque Estadual do Desengano, RJ | 03/17/08 | KC608277 | |
Choeradoplana sp. (in |
F4063 |
|
– | Parque Estadual do Desengano, RJ | 08/12/09 | KF971679 |
Tissue of the only Ch. eudoxiae Silva & Carbayo, sp. nov. individual was depleted during attempts to sequence it. COI sequences were obtained from the remaining ten specimens representing the three other new species, and Ch. tristriata and Ch. albonigra. Sequence alignments resulted in a matrix with 54 terminals and 679 base pairs. PartitionFinder indicated two partitions (first and second codon positions and third codon position), each with a different evolutionary model, with the TIM substitution model having gamma-distributed rate variations across sites and a proportion of invariable sites (TIM + I+ G) for the first and second codons, and a GTR substitution model with gamma-distributed rate variation across sites and a proportion of invariable sites (GTR + I + G) for the third codon partition.
Phylogenetic analyses under the two optimality criteria (BI and ML) retrieved the genus Choeradoplana and all morphological species as monophyletic with high posterior probabilities and bootstrap value, respectively (Fig.
Subfamily Geoplaninae Stimpson, 1857
Choeradoplana Graff, 1896
Geoplana tristriata Schultze & Müller, 1857: 23.
Not Geoplana tristriata in
Pseudogeoplana tristriata: Ogren & Kawakatsu, 1990: 161.
Municipality of Blumenau and Parque Estadual da Serra de Tabuleiro, State of Santa Catarina, Brazil.
Choeradoplana species with yellow green background color, with three thin discontinuous longitudinal black lines; ventral side is zinc-yellow. Copulatory apparatus compact, without penis papilla; female atrium funnel-shaped.
The preserved specimen measures 22 mm long and 2.5 mm wide (Fig.
The dorsal coloration consists of a yellow green (RAL 1018) background color, with three thin discontinuous longitudinal lines of small black spots. These spots are less concentrated in the median line (Fig.
The eyes are formed by one pigmented cup of 80 μm in diameter (Fig.
Sensory pits are 25 μm deep (Fig.
Numerous rhabditogen cells discharge through the glandular cushions of the cephalic region. These cells are scarce in the dorsal epidermis. Abundant erythrophil gland cells pierce the dorsal and marginal epithelium in the pre-pharyngeal region. The entire epithelium is additionally pierced by scarce gland cells of two types, producing cyanophil and xanthophil granules, respectively. No glandular margin.
The cutaneous musculature of the pre-pharyngeal region comprises a subepithelial circular muscle, followed by a diagonal layer with decussate fibers, and a longitudinal muscle organized in tight bundles (Figs
There are three parenchymal muscle layers in the pre-pharyngeal region (Fig.
The ventral longitudinal cutaneous muscle is modified into the retractor muscle in the cephalic region. This retractor muscle is delta-shaped in cross-section along 0.7 mm (or 3% of body length), starting 0.2 mm (or 1%) from the anterior extremity of the body (Fig.
Phylogenetic tree of Choeradoplana obtained from the COI gene by Bayesian inference. Black numbers at the nodes correspond to the posterior probability (only values above 0.99 shown) and blue numbers to Bootstrap support in the tree by maximum likelihood (only values above 95% shown). See text for details.
The mouth is located in the middle of the pharyngeal pouch (Fig.
The testes are dorsal, located between the intestinal diverticula, with some of them reaching the parenchymal supra-intestinal transverse muscle (Figs
Choeradoplana tristriata (Schultze & Müller, 1857), specimen F3226 A dorsal view of the live specimen B lateral view of the anterior region of the live specimen C photomicrograph of a transverse section of the cephalic region, showing an eye and a sensory pit (arrowhead) D photomicrograph of a transverse section of the pre-pharyngeal region. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
The male atrium is long and narrow with folded walls. The proximal third of the atrium runs postero-dorsally; distal two-thirds runs ventrally almost vertically above the gonopore canal. The atrium is lined by a cuboidal-non-ciliated epithelium, and underlain by an 80 μm-thick circular muscle with interspersed longitudinal fibers. The male atrium is 1.2× longer than the female atrium.
Choeradoplana tristriata (Schultze & Müller, 1857), specimen F3226. Photomicrographs of transverse sections A dorsal portion of the pre-pharyngeal region B ventral region of the pre-pharyngeal region C cephalic region. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
The ovaries are mature, ovoid, and 200 μm in length. They are located above the ventral nerve plate at a distance from the anterior body tip equal to 25% of its body length (5.5 mm from anterior tip). Ovovitelline ducts emerge from the dorso-lateral aspect of the ovaries, where-after they run backwards above the ventral nerve plate. The ducts bend medially, posteriorly to the female atrium, and subsequently ascend vertically and medially to communicate with each other above the postero-dorsal section of the female atrium (Fig.
The female atrium is funnel-shaped, not folded, and lined by a ciliated columnar-to-cuboidal epithelium, which is surrounded by circular muscle fibers with interspersed longitudinal fibers. This muscle is continuous with the common muscle coat. Most of the abundant gland cells discharging into the female atrium have a fine granular xanthophil and erythrophil secretion. The length:height ratio of the copulatory apparatus enveloped by the common muscle coat is 1.4:1.
Choeradoplana tristriata (Schultze & Müller, 1857), specimen F3226 A photomicrograph of a sagittal section of the pharynx B photomicrograph of a sagittal section of the copulatory apparatus C diagrammatic representation of the copulatory apparatus. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
On the identity of our specimen.
There is no record of the deposition of the type series. It was probably not preserved. Our specimen was collected 115 km south from the type locality, and matches Schultze and Müller’s species in all characteristics. The conspecificity of our specimen could be questioned since the copulatory apparatus is the most important organ assuring identification in triclads. However, this species combines a set of unusual features among Geoplanins: the color pattern of the body, the cephalic region bent to the dorsal side (actually only found in Choeradoplana and Cephaloflexa among Geoplaninae), and the absence of eyes in the very anterior tip of the body. Schultze and Müller’s and our specimen sharing these uncommon attributes supports their conspecificity.
The species redescribed herein also matches all diagnostic characteristics of Choeradoplana and should therefore be transferred to this genus. The species is unique in the external aspect in that there are no other species of Choeradoplana with dorsal green color with three longitudinal dark stripes. Internally, Choeradoplana bilix Marcus, 1951; Ch. crassiphalla Negrete & Brusa, 2012; Ch. langi (Dendy, 1894); and Ch. marthae Froehlich, 1955 are similar to Ch. tristriata in the compact aspect of the copulatory apparatus, having a length:height ratio equivalent to 1.8:1 or less, as calculated in drawings (
The identity of Graff’s specimen and subsequent taxonomic actions. Herman von Ihering collected one specimen in Taquara, State of Rio Grande do Sul, Brazil, which he identified as a member of this species. Ihering sent it to
Choeradoplana tristriata (Schultze & Müller, 1857), specimen F3226. Photomicrographs of sagittal sections A prostatic vesicle and the male atrium B female atrium. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
We did not find Graff’s specimen in the museums where part of this collection was disseminated (Naturhistorisches Museum, Basel; Museum of Natural History, Vienna; Senckenberg Museum, Frankfurt; Zoological Museum, Hamburg; Natural History Museum, London). Therefore, we consider Graff’s specimen lost.
Geoplana albonigra Riester, 1938: 7–9, figs 4, 5, 86, 87, taf. 1, fig. 2.
Notogynaphallia albonigra: Ogren & Kawakatsu, 1990: 140.
Choeradoplana albonigra:
Holotype
Reserva Biológica Augusto Ruschi, municipality of Santa Teresa, State of Espírito Santo, Brazil. May 26–27th, 2008.
Parque Estadual do Desengano, municipality of Santa Maria Madalena, State of Rio de Janeiro, Brazil. August 10–13th, 2009.
Reserva Biológica Augusto Ruschi, Santa Teresa, State of Espírito Santo; Parque Estadual do Desengano, Santa Maria Madalena, State of Rio de Janeiro; Municipality of Teresópolis, State of Rio de Janeiro, Brazil.
Choeradoplana species with a white dorsum, covered by a wide median black band, darker at its margins; an additional thin black median stripe may be present. The anterior third of the body is progressively thinner towards the pointed tip; its extremity has no lateral dilations or “neck” differentiating the head from the body. The ventral side of the cephalic region is concave and without glandular cushions. The proximal third of the prostatic vesicle is extrabulbar. The copulatory apparatus is relatively long; penis papilla is absent, and the female atrium is approximately funnel-shaped.
Living specimens range between 50–63 mm in length and 2–3 mm in width (n = 2). Preserved specimens range between 45–73 mm in length and 2–4 mm in width (n = 4). The body is slender and subcylindrical, with the anterior third becoming progressively thinner to the anterior tip. The anterior extremity is very thin and coiled up so that the ventral surface is facing out (Fig.
Choeradoplana albonigra (Riester, 1938) A habitus of living specimen F4024 in dorsal view B detail of anterior extremity of living specimen F2313 in dorsal view. Debris is glued on the body C detail of anterior extremity of living specimen F4024 in lateral view D detail of anterior extremity of preserved specimen F4031 in ventral view. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
The background color of the body is traffic white (RAL 9016). It is dorsally covered by a wide graphite black (RAL 9011) band, darker at its margins, as wide as three-quarters of the body width, in the middle of which runs a thin jet black (RAL 9005) stripe which is not apparent in some individuals. Anterior and posterior extremities of the body are slightly orangish. The color has faded out in preserved specimens. The dorsal graphite black band in the body tips of the holotype split into two brownish stripes.
The eyes are of one-pigment cup type, 25–45 µm in diameter; with no clear halos. They are marginally distributed in an irregular row of 2–6 eyes, from the anterior tip of the body (Figs
The sensory pits are 22–27 μm deep and ventro-laterally are distributed in a single row along approximately the anterior one-seventh of the body. The pits are absent at the very anterior tip of the body (300 µm).
Numerous rhabditogen cells open onto the dorsal surface of the body (Fig.
The cutaneous musculature consists of a subepithelial circular muscle, followed by a diagonal layer with decussate fibers, and a strong longitudinal muscle organized in bundles (Fig.
The pre-pharyngeal region, namely the dorsal decussate muscle (40–55 μm thick, n = 2), transverse supra-intestinal muscle (74–100 μm); and transverse subintestinal muscle (45–65 μm) (n = 2) (Fig.
The retractor muscle of the head is delta-shaped in a cross-section along 0.3 mm (or 0.5% of body length) from behind, 0.1 mm (or 0.15%) of the anterior extremity of the body (Fig.
The mouth is located at a distance from the anterior section of the pharyngeal pouch ranging between 55.1–78.9% (n = 4) (Fig.
The testes are dorsal, located under the supra-intestinal transverse muscle layer, partially placed between the intestinal diverticula. They extend from the level of the ovaries (a distance from the anterior extremity of the body equal to 27% of the body length) to nearly the root of pharynx (53% of the body length). Sperm ducts run immediately above the subintestinal muscle layer, dorsally and slightly laterally to the ovovitelline ducts. Distal portions of sperm ducts contain sperm, and are surrounded by a circular muscle. Sperm ducts communicate with the two roughly horizontal branches of the extrabulbar portion of the prostatic vesicle. These branches open laterally into an irregular, pear-shaped cavity, which is located more or less under the anterior section of the penis bulb (Figs
Choeradoplana albonigra (Riester, 1938) A diagrammatic transverse section of a portion, seemingly near the anterior extremity, of holotype. Photomicrographs of transverse sections (B–F) B dorsal epidermis in pre-pharyngeal region of specimen F4024 C ventral epidermis in pre-pharyngeal region of specimen F4024 D–F cephalic region of specimen F4081 at 1.2, 0.4, and 0.15 millimeters from anterior extremity of the body, respectively. Scale bar: 200 µm. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
The proximal half of the male atrium is slightly folded and narrow. The distal half is ample and is narrowed distally by a large, dorsal fold extending through both the male and female atria. The stroma of this fold is strongly muscularized with longitudinal and oblique fibers. Additional lateral folds may be present in the distal half (Figs
Choeradoplana albonigra (Riester, 1938) A diagrammatic representation of the pharynx from sagittal sections of holotype B sagittal section of the copulatory apparatus of specimen F2391; note the small finger-shaped fold of the male atrium (arrow) C photomicrograph of a sagittal section of the copulatory apparatus of specimen F4024. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
The proximal half of the male atrium is lined with a 5 μm high non-ciliated, infra-nucleated epithelium which is pierced by scarce gland cells producing fine erythrophil granules, and by gland cells producing variously sized xanthophil granules. This epithelium is surrounded by a 20–60 μm-thick dense muscle of very thin muscle fibers (2 μm); followed by a muscle (< 150 μm thick) of 4 μm-thick fibers. The distal half of the male atrium is lined with an epithelium which is pierced by gland cells producing erythrophil granules. An intensely reddish erythrophil is found beneath this epithelium secretion. The lining epithelium of the distal half of the male atrium is surrounded by a circular muscle (18–45 μm); followed by a longitudinal muscle (80–150 μm) (n = 3).
Choeradoplana albonigra (Riester, 1938) A diagrammatic reconstruction of copulatory apparatus of holotype from sagittal sections B photomicrograph of a sagittal section of the unpaired portion of the prostatic vesicle and proximal section of male atrium of specimen F4024. Arrow points the small ring-shaped horizontal fold communicating prostatic vesicle with male atrium C diagrammatic reconstruction of copulatory apparatus of specimen F4081 from sagittal sections D photomicrograph of a sagittal section of the female atrium of specimen F4081. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
A spermatophore is in the stroma of the large dorsal fold leveled with the gonopore in three specimens (F2391, F4024, F4081) (Fig.
The ovaries are mature, very elongated, and club-shaped due to the dilated proximal extremity. The thin portion can be divided into smaller segments. The size of the ovaries ranges between 700–1200 µm in length and 120–170 µm in width (n = 4). They are located above the ventral nerve plate, and at a distance from the anterior extremity equal to 27.1–31.3% of the body length (n = 2). Ovovitelline ducts emerge from the dorso-lateral aspect of the ovaries and run above the nerve plate. The proximal segment of the oviducts is dilated and contains sperm (n = 4). They ascend posteriorly and medially laterally to the female atrium, then unite dorsally to the common glandular ovovitelline duct (Fig.
The female atrium is lined with a columnar, non-ciliated epithelium, and is pierced by two types of cells producing erythrophil and cyanophil granular secretions, respectively. The female atrium is as long as half the male atrium. The common muscular coat of the copulatory apparatus is composed of a weak layer of intermingled fibers; it is 20–40 μm thick in the anterior section, and thinner in the posterior section. The length:height ratio of the copulatory apparatus enveloped by the common muscle coat ranges between 3.0–3.5:1 (n = 5; mean 3.2:1).
Creeping on the Petri dish, the animals sometimes rise up to three-quarters of the body from the substrate and swing to the sides as they would be searching for ground. When touched, they can react by tumbling. A similar behavior, named ‘escape reaction’, was observed for Ch. marthae by
This species was originally described as Geoplana albonigra Riester, 1938, from Teresópolis, State of Rio de Janeiro, Brazil. The external aspect and the internal morphology of the pharynx and copulatory apparatus were given in the original description. The species was later transferred to the recently proposed new genus Notogynaphallia Ogren & Kawakatsu, 1990, erected for species of Geoplaninae without penis papilla and dorsally located female genital canal. Based on morphological and molecular information,
On the identity of our specimens. Our specimens and the holotype of Ch. albonigra are much alike, with the exception of the size of the male and female atria. Whereas the male and female atria are relatively narrow in the holotype, these atria are higher in two out of four mature individuals. Differences of the same nature have been observed in other land planarians (e.g., Pasipha pasipha (Marcus, 1951); Obama josefi (Carbayo & Leal-Zanchet, 2001)), and this might be caused by different states of maturation of each specimen, albeit all being mature, or by the physiological state of the individuals such as a recent copulation, as seems to be the case of the specimens bearing a spermatophore.
The systematic position of Ch. albonigra. Riester described the species from a single individual and assigned the species to Geoplana. In Riester’s description, there is no reference to the inner structures of the cephalic region, nor to the cutaneous muscle coat. The cephalic region of the holotype is embedded in Canada balsam on a histological glass slide. Our study revealed a set of additional aspects, including the delta-shaped retractor muscle of the head and the in-sunk ventral longitudinal cutaneous muscle which only agree with Choeradoplana. Our molecular data also support this conclusion. However, Ch. albonigra deviates from the genus in the body shape, since its anterior third narrows progressively towards the anterior extremity, with the latter also lacking the typical glandular cushions of Choeradoplana. Accordingly, the diagnosis of the genus is revised below.
Holotype
Only known from the type locality, Floresta Nacional de São Francisco de Paula, State of Rio Grande do Sul, Brazil.
The specific epithet pays homage to the late Prof. Eudóxia Maria Froehlich, 21 October 1928 – 26 September 2015, for her insightful life lessons and lasting contribution to the knowledge of the neotropical planarian fauna for 60 years.
Choeradoplana species with pastel yellow back and brown fawn spots more concentrated in the paramedian region. Its anterior extremity has no lateral dilations or “neck” differentiating its head from its body. The ventral side of the cephalic region is concave, and without distinct glandular cushions. The extrabulbar portion of the prostatic vesicle has paired branches and an unpaired, roughly rounded section; the intrabulbar portion is a dilated vertical duct. Penis papilla is absent.
The live holotype measured 38 mm in length, and 1.5 mm in width. Preserved, it measured 27.5 mm in length and 2 mm in width. Its body is slender and subcylindrical, with the anterior 1/8 becoming progressively thinner towards the anterior tip. The anterior extremity is rounded and the posterior is pointed. The dorsal side is convex, while the ventral side is slightly convex. The anteriormost body portion is approximately five millimeters long and rolled up so that the ventral side is facing upwards (Fig.
The dorsum background color of the body is pastel yellow (RAL 1034) with fawn brown (RAL 8007) spots (Fig.
The eyes are one pigmented-cup type of 25–30 µm in diameter. There are no clear halos around them (Fig.
Sensory pits are 17.0–22.5 µm deep, distributed ventro-laterally in a uniserial row from the anterior sections of the body (approximately 0.2 mm of the anteriormost body were lost) to 4.5 mm behind it.
Abundant rhabditogen cells open onto the dorsal surface of the body and its margins in the pre-pharyngeal region. The epithelium of the margins is also pierced by gland cells producing erythrophil granules (Fig.
The cutaneous musculature consists of a subepithelial circular muscle, followed by a diagonal layer with decussate fibers, and a longitudinal muscle organized in bundles (Fig.
In the pre-pharyngeal region, the same parenchymal muscles as in Ch. iheringi, namely the dorsal decussate muscle (52–55 μm thick), transverse supra-intestinal muscle (20–22 μm); and transverse subintestinal muscle (12–15 μm) (Fig.
The muscle retractor of the head is delta-shaped in a cross-section along ~ 0.5 mm (or 1.8% of body length) starting from 0.1 mm behind the anterior extremity of the body (Fig.
The central nervous system presents a ventral nerve plate (70–85 μm thick or 9–11% of body height) in the pre-pharyngeal region.
The mouth is located in the middle of the pharyngeal pouch (Fig.
The testes are dorsal, 90–150 μm in diameter, located under the supra-intestinal transverse muscle layer, and partially placed between the intestinal diverticula. The anteriormost testes are located 0.9 mm anterior to the ovaries (or 21% of the body length); posteriormost near the root of the pharynx (49% of the body length). Sperm ducts run immediately above the subintestinal muscle layer, dorsally and slightly internal to the ovovitelline ducts. Distal portions of sperm ducts contain sperm and are surrounded by a 20 μm-thick circular muscle. These ducts communicate with the respective short branch of the prostatic vesicle (Fig.
Choeradoplana eudoxiae Silva & Carbayo, sp. nov. Holotype A living animal in dorsal view B, C detail of anterior extremity in a dorsal view D detail of anterior extremity in ventro-lateral view in the preserved specimen. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
The male atrium is elongated. The proximal half is horizontal, slightly folded and narrow. The distal half is wider, and provided with two large transverse and oblique folds. The atrium is lined with a 7 μm high epithelium, and pierced by two types of gland cells producing erythrophil and cyanophil granules, respectively. The atrial epithelium is underlain by a 20 to 35 μm-thick circular muscle with longitudinal fibers intermingled (Figs
Choeradoplana eudoxiae Silva & Carbayo, sp. nov. Photomicrographs of transverse sections of the holotype A dorsal portion of the pre-pharyngeal region ofreion B ventral portion of the pre-pharyngeal region C anterior region at 0.1 mm from the anterior tip of the body. of the pre-pharyngeal region D anterior region at 0.5 mm from the anterior tip of the body. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
The ovaries are mature, rounded, ~ 100 µm in diameter. They are located 8.9 mm from the anterior extremity of the body (24.7 % of body length), and above the ventral nerve plate. The ovovitelline ducts emerge from the dorso-lateral aspect of the ovaries and run above the nerve plate; their proximal section contains sperm. Laterally to the female atrium, they rise posteriorly to unite dorsally to the common glandular ovovitelline duct (Fig.
Choeradoplana eudoxiae Silva & Carbayo, sp. nov. Photomicrographs of sagittal sections of holotype A, B pharynx C prostatic vesicle and male atrium D copulatory apparatus. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
Choeradoplana eudoxiae Silva & Carbayo, sp. nov. Holotype A diagrammatic reconstruction of copulatory apparatus B photomicrograph of a sagittal section of the female atrium. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
The female atrium is irregular, provided with two or three lateral and dorsal folds (Fig.
The common muscular coat is well developed and continuous with the penis bulb. This coat wraps the intrabulbar portion of the prostatic vesicle, and the male and female atria. The length:height ratio of the copulatory apparatus enveloped by the common muscle coat is 2.2:1.
When touched with a finger on the posterior end, the animal reacted by rolling forward. Firstly, it lifted its posterior extremity forward to touch the ground at the level of the midbody so that the body forms a loop. Next, the loop moved forwards until the anterior third of the body detached from the ground, which subsequently lengthened and touched the substrate. By doing so, the animal moved forward a distance equivalent to half its body length in approximately one second. It then immediately repeated this whole movement repeatedly.
The species described herein matches all diagnostic characteristics of Choeradoplana, except for the glandular cushions of the cephalic region, which are not developed. This is so notable that the species was initially assigned to Cephaloflexa upon examination of the live and preserved specimen. Regarding the body shape, Cephaloflexa is characterized by having “the anterior third very gradually narrowing, without constriction or widening and without grooves on the ventral surface. The anterior tip rolled upwards and is ventrally concave” (
The remaining diagnostic attributes of Choeradoplana are present in Ch. eudoxiae Silva & Carbayo, sp. nov., such as the ventral cutaneous longitudinal muscle partially sunken into the parenchyma; a retractor muscle of the cephalic extremity with a delta shape in transverse section; and a dorsal decussate parenchymatic muscle modified in the cephalic region into the Muskelgeflecht.
The body color of the Ch. eudoxiae Silva & Carbayo, sp. nov. resembles that of some congeners in the brownish background color with dark black or dark brown spots over it, namely Choeradoplana abaiba
With respect to the internal morphology, Ch. eudoxiae Silva & Carbayo, sp. nov. is similar to Ch. albonigra, Ch. tristriata, Ch. bocaina, Ch. riutortae Lago-Barcia & Carbayo, sp. nov., Ch. claudioi Lago-Barcia & Carbayo, sp. nov., and Ch. onae Lago-Barcia & Carbayo, sp. nov. in that the prostatic vesicle is extrabulbar and it is lacking a penis papilla. However, in the latter four species an extrabulbar portion of the prostatic vesicle is dish-shaped, whereas this organ is pear-shaped (in Ch. eudoxiae Silva & Carbayo, sp. nov.) or has two short tubular branches (branches (with a pear-shaped organ) Ch. tristriata (paired tubes) and Ch. albonigra). Ch. eudoxiae sp. nov. is distinguished from Ch. tristriata in the relatively compact copulatory apparatus of the latter, and from Ch. albonigra in that the copulatory apparatus in this species is relatively longer, the paired portions of the prostatic vesicle are shorter, and the common glandular ovovitelline duct is relatively shorter.
Both specimens were collected in Reserva Biológica Augusto Ruschi, Santa Teresa, State of Espírito Santo, Brazil (-19.8891, -40.5459) by F. Carbayo and co-workers, May 27–29th, 2008; Holotype
Only known from the type locality, Reserva Biológica Augusto Ruschi, Santa Teresa, State of Espírito Santo, Brazil.
The specific epithet honors Prof. Claudio Gilberto Froehlich for his contributions to the knowledge of the Neotropical land planarians.
Choeradoplana species with a golden yellow background color, with scattered sepia brown speckles on the whole dorsal surface, except for the anterior, greyish extremity. The extrabulbar portion of the prostatic vesicle is dish-like. The female genital atrium is compressed dorso-ventrally and partially positioned below the distal section of the male atrium.
Preserved specimens measure 24.0–36.5 mm in length and 2.5–3.0 mm in width (n = 2). The body is slender and subcylindrical. The cephalic region is differentiated from the remaining body by a ‘neck’, laterally dilated and rolled up so that the ventral surface provided with glandular cushions faces out; the posterior extremity is pointed. The creeping sole is as wide as 75% (F2424) of the body width at the pre-pharyngeal region. The mouth is positioned at a distance from the anterior extremity equal to 50% of the body length, and the gonopore is at 60%.
The dorsal coloration of the live specimens consists of a golden yellow (RAL 1004) background color, with scattered sepia brown (RAL 8014) speckles on the whole dorsal surface, except for the anterior, greyish extremity (Fig.
Its eyes are devoid of halos and are formed by a one-pigmented cup of 60 μm in diameter. Eyes are absent in the very anterior extremity of the body equivalent to more or less 1% of the body length. The eyes are distributed marginally in a row of two or three eyes along the first 4.5 mm (or 12% of body length), then they are arranged in a single marginal row until the posterior end.
The sensory pits are 15 µm deep, and are distributed ventro-laterally in a uniserial row, only starting at approximately the equivalent to 1% of body length. The ventral epithelium of the ovarian region was lost and sensory pits are absent in the pre-pharyngeal region.
The cutaneous musculature of the pre-pharyngeal region consists of a subepithelial circular muscle followed by a diagonal layer with decussate fibers, and a strong longitudinal muscle organized in bundles (Fig.
In the pre-pharyngeal region, a dorsal decussate muscle (25 μm thick), transverse supra-intestinal muscle (25 μm); and transverse subintestinal muscle (15 μm) (n = 1) (Fig.
The cutaneous and parenchymal musculature is organized in the cephalic region as in Ch. iheringi. The muscle retractor of the head is delta-shaped in a cross-section along 1.8 mm (or 5% of body length, F2424) from behind, 1.3 mm (or 4%, F2424) of the anterior extremity of the body (Fig.
The mouth is located in the middle of the pharyngeal pouch (Fig.
Choeradoplana claudioi Lago-Barcia & Carbayo, sp. nov., holotype A dorsal view of the creeping live animal B photomicrograph of a transverse section of the pre-pharyngeal region C photomicrograph of a transverse section of the cephalic region D photomicrograph of a sagittal section of the pharynx. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
The testes are mature, dorsal, arranged in four paramedian rows between the supra-intestinal transverse parenchymal muscle and the intestinal diverticula (Fig.
The male atrium is 5–6× longer than the female atrium, and divided into a dorsal, proximal narrow third, slightly folded, and a distal two-thirds portion with some smaller folds. A main, very large, oblique fold on each side of the body extends behind the gonopore level and over the female atrium (Fig.
The ovaries are mature, very elongated and placed above the ventral nerve plate at a distance from anterior tip of the body equal to 21% of body length (7.7 mm from anterior tip) (holotype). They present an anterior, ovoid section, 300 μm in length (F2424), and a posterior, 600 µm (F2424) long narrow section (Fig.
The female atrium is dorso-ventrally compressed and wider towards the gonopore canal. It is placed below the posterior section of the male atrium (Fig.
Choeradoplana claudioi Lago-Barcia & Carbayo, sp. nov. A photomicrograph of a sagittal section of the copulatory apparatus of holotype B photomicrograph of a sagittal section of the copulatory apparatus of paratype F2510 C diagrammatic representation of the copulatory apparatus of holotype D photomicrograph of a sagittal section of the prostatic vesicle of holotype E photomicrograph of a sagittal section of the ovarian region of holotype F photomicrograph of a sagittal section of the female atrium of holotype. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
The common muscle coat is a very dense layer composed by variously oriented muscle fibers. The length:height ratio of the copulatory apparatus enveloped by the common muscle coat ranges between 2.5–2.8:1.
Ch. claudioi Lago-Barcia & Carbayo, sp. nov. externally differs from most congeners in that the dorsum is composed of a light background color evenly covered with brown spots. However, this color pattern is so similar to Ch. abaiba, Ch. agua, Ch. banga, Ch. iheringi, and Ch. pucupucu that Ch. claudioi Lago-Barcia & Carbayo, sp. nov. cannot be confidently distinguished from them.
With respect to the internal morphology, Ch. claudioi Lago-Barcia & Carbayo, sp. nov. can be differentiated from most Choeradoplana species by the dish-shaped portion of the extrabulbar region of the prostatic vesicle. This attribute is only shared with Ch. onae Lago-Barcia & Carbayo, sp. nov., Ch. riutortae Lago-Barcia & Carbayo, sp. nov., and Ch. bocaina. However, the female genital atrium is compressed dorso-ventrally and partially positioned below the distal section of the male atrium, which readily distinguishes Ch. claudioi Lago-Barcia & Carbayo, sp. nov. from these three other species.
Choeradoplana
sp. in
All specimens collected in the Reserva Biológica Augusto Ruschi, Santa Teresa, State of Espírito Santo, Brazil (-19.88, -40.54) by F. Carbayo and co-workers, 25–27 May 2008; Holotype
Only known from the type locality, Reserva Biológica Augusto Ruschi, Santa Teresa, State of Espírito Santo, Brazil.
The name onae is the affectionate nickname of the biologist Marta Álvarez-Presas (Bristol University). The specific epithet honors her for her contributions to understanding the systematics of free-living flatworms.
Choeradoplana species with a light ivory background color and a wide sepia brown median band. The extrabulbar region of the prostatic vesicle has a dish-shaped portion. The copulatory apparatus is 3.8× longer than its height. The male atrium has 4–6 main folds.
External aspect. Preserved specimens range between 41–44.5 mm in length and 3–4 mm (n = 4) in width. The body is slender and subcylindrical. The cephalic region is differentiated from the remaining body by a ‘neck’ and laterally dilated. This region is rolled up so that the ventral surface provided with two prominent glandular cushions is facing out when alive (Fig.
The dorsal coloration of live specimens consists of a light ivory (RAL 1015) background color (Fig.
Choeradoplana onae Lago-Barcia & Carbayo, sp. nov. A dorsal view of the creeping live paratype F2230 B live paratype F2310 rolled up showing the ventral surface C lateral view of the cephalic region of live paratype F2230 D photomicrograph of a transverse section of the pre-pharyngeal region of holotype E photomicrograph of a transverse section of the cephalic region of holotype. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
The eyes are devoid of halos, and formed by a one-pigmented cup of 60 μm in diameter. Eyes are absent in the very anterior extremity of the body equivalent to 1% of the body length (n = 1). Eyes behind the anterior tip are distributed marginally in a row of two or three eyes (Fig.
Sensory pits are 20–25 µm deep in a uniserial ventro-lateral row, starting from 0.4 mm behind the anterior extremity, the equivalent of 1% body length to at least 80 mm from the anterior tip (20% of body length, n = 1).
Rhabditogen gland cells pierce the marginal epidermis in the pre-pharyngeal region. Erythrophil granules and scarce cyanophil granules are discharged through the entire epidermis. There is no glandular margin (Fig.
The cutaneous musculature consists of a subepithelial circular muscle, followed by a diagonal layer with decussate fibers, and a strong longitudinal muscle organized in bundles (Fig.
In the pre-pharyngeal region, there are three parenchymal muscles, namely a dorsal decussate muscle (40–50 μm thick), a transverse supra-intestinal muscle (15 μm); and transverse subintestinal muscle (18–20 μm) (n = 4) (Fig.
The cutaneous and parenchymal musculature is organized in the cephalic region as in Ch. iheringi. The muscle retractor of the head is delta-shaped in a cross-section along 2.5 mm (or 6% of body length) from behind, 0.9 mm (or 2%) anterior extremity of the body (Fig.
The mouth is located in the middle of the pharyngeal pouch (n = 4) (Fig.
The testes are mature, dorsally located under the supra-intestinal transverse parenchymal muscle, placed between the intestinal diverticula. They extend from 13.2 mm (32% of body length, holotype) from the anterior extremity to 0.2 mm of the root of the pharynx (63%, holotype). Sperm ducts bend dorsally and medially immediately above the subintestinal parechymatic muscle layer to open into the respective dilated branch of the prostatic vesicle. The prostatic vesicle is divided into two halves (Fig.
Choeradoplana onae Lago-Barcia & Carbayo, sp. nov. Photomicrographs of sagittal sections A pharynx of paratype F2230 B pharynx and copulatory apparatus of holotype C prostatic vesicle of paratype F2230 D prostatic vesicle of holotype. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
The male atrium is long, 5× as long as the female atrium, with the same height along its length and 4–6 large transverse folds narrowing its lumen. The male atrium is lined by a cuboidal, non-ciliated epithelium, and is underlain by a 40–70 µm-thick circular muscle with numerous interspersed longitudinal fibers (n = 4). The proximal two thirds of the atrium receive two types of abundant gland cells producing xanthophil and erythrophil granules, respectively, and a third type of scarce gland cells producing amorphous xanthophil secretion; the distal third of the male atrium receives abundant gland cells producing erythrophil granules. The sub-apical portion of the cells of the lining epithelium of this distal third contains xanthophil granules.
The ovaries are mature, ovoid, 250 μm in length, placed above the ventral nerve plate and at a distance from the anterior tip of the body equal to 28% of body length (11.8 mm from the anterior tip) (n = 1). Ovovitelline ducts emerge from the dorso-lateral aspect of the ovaries and run ventrally. Ovovitelline ducts run medially and dorsally lateral to the posterior section of the female atrium, then unite above the postero-dorsal section of the female atrium (Fig.
The female atrium is funnel-shaped, and is lined with a 50 µm high epithelium, which is pierced by gland cells producing fine erythrophil granules. The subapical portion of the lining cells contains xanthophil granules. The lining epithelium of the female atrium is underlain by a 1-fiber-thick longitudinal muscle, followed by a 10 µm-thick layer of decussate muscle fibers. Paratype F2281 presents a female atrium smaller than that of the remaining specimens and also bears a spermatophore at the entrance of the gonopore canal. This spermatophore is ovoid, and with approximately 100 µm in maximum diameter. It is constituted on an inner mass of sperm surrounded by a thin fibrous, erythrophil layer, external to which is a gross layer of xanthophil, granular secretion and a bluish fine granular secretion, each prevailing on one side of the spermatophore (Fig.
The common muscle coat is a very dense layer composed by variously oriented muscle fibers. The length:height ratio of the copulatory apparatus enveloped by the common muscle coat ranges between 2.5–3.3:1 (n = 3).
The species described herein matches all diagnostic characteristics of Choeradoplana. As reported for Ch. claudioi Lago-Barcia & Carbayo, sp. nov., Ch. onae Lago-Barcia & Carbayo, sp. nov. only resembles Ch. abaiba, Ch. agua, Ch. banga, Ch. iheringi, Ch. claudioi Lago-Barcia & Carbayo, sp. nov., and Ch. pucupucu in the body color. The great similarity between them hinders confident identification. However, none of them present the prominent cushions found in this species with a red-orange color.
With respect to the internal morphology, Ch. onae Lago-Barcia & Carbayo, sp. nov. only compares with Ch. riutortae Lago-Barcia & Carbayo, sp. nov. and Ch. bocaina in that they also present a dish-shaped prostatic vesicle. However, the length:height ratio of the copulatory apparatus in these species is 2.6:1 (vs. 3.8:1 in Ch. onae Lago-Barcia & Carbayo, sp. nov.); the male atrium:female atrium ratio in Ch. bocaina and Ch. riutortae Lago-Barcia & Carbayo, sp. nov. ratio ranges between 1:1–3:1 (Carbayo & E. M. Froehlich, 2012), whereas it is ~5:1 in Ch. claudioi Lago-Barcia & Carbayo, sp. nov. and Ch. onae Lago-Barcia & Carbayo, sp. nov., and the male atrium presents 1–2 large folds (vs. 4–6 in Ch. onae Lago-Barcia & Carbayo, sp. nov.).
Choeradoplana onae Lago-Barcia & Carbayo, sp. nov. A photomicrograph of a sagittal section of the copulatory apparatus of paratype F2230 B photomicrograph of a sagittal section of the copulatory apparatus of holotype C diagrammatic representation of the copulatory apparatus of paratype F2230 D photomicrograph of a sagittal section of the entrance of the gonopore of paratype F2281 housing a spermatophore. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
All specimens were collected in the Parque Nacional da Serra dos Orgãos, Teresópolis, State of Rio de Janeiro, Brazil (-22.48, -43.06) by F. Carbayo and co-workers, January 6th, 2010. Holotype
Only known from the type locality, Parque Nacional da Serra dos Orgãos, municipality of Teresópolis, State of Rio de Janeiro, Brazil.
The specific epithet honors Prof. Marta Riutort for her contributions to understanding the evolution of flatworms.
Choeradoplana species with a light ivory background color covered by numerous sepia brown spots except for the anterior extremity which is red orange. The ventral surface is pale orange in the cephalic region, and light grey in the rest of the body. Part of the longitudinal cutaneous musculature is sunken in the parenchyma of the ventral side. The prostatic vesicle has a paired extrabulbar dish-shaped portion, and an elongated intrabulbar portion with an irregular epithelium. It has a short copulatory apparatus (the length:height ratio of the copulatory apparatus is 2.6:1). The male atrium presents the same size as the female atrium.
The preserved animals measure between 37–42 mm in length and 2.5–3 mm in width (n = 3). The body is slender and subcylindrical. The cephalic region is differentiated from the remaining body by a ‘neck’, laterally dilated and rolled up so that the ventral surface, provided with prominent glandular cushions, is facing out (Fig.
The dorsal coloration in live specimens consists of a light ivory (RAL 1015) background color, with numerous sepia brown (RAL 8014) spots which are more (F4218) or less (F4217) merged with each other, with the latter situation presenting a somewhat homogeneous aspect. A midline with the background color may extend along the body length (paratype F4217) or is restricted to the anterior region of the body (paratype F4261). The spots extend to the body sides, where they are scattered so as to create an irregular bordering line, followed by the background color of the sides of the body. A curled anterior extremity is red orange (RAL 2001). The ventral surface is pale red orange in the cephalic region, and light grey (RAL 7035) in the rest of the body (Fig.
The eyes are formed by a one-pigmented cup of 46–50 μm in diameter. There are no halos around them. Eyes are absent in the very anterior extremity of the body equivalent to 1% of the body length (F4218). Eyes behind the anterior tip are distributed marginally in a row of two or three eyes and extend along the entire body until the posterior extremity.
Choeradoplana riutortae Lago-Barcia & Carbayo, sp. nov. A dorsal view of the creeping live paratype F4217 B the live holotype twisted showing the ventral surface C dorsal view of the anterior region of paratype F4217 D photomicrograph of a transverse section of the pre-pharyngeal region of holotype E photomicrograph of a transverse section of the cephalic region of holotype. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
Sensory pits are 15 μm deep, distributed ventro-laterally in a uniserial row initiating 0.3 mm behind the anterior extremity (the equivalent of 1% of the body length in paratype F4217), and from the very anterior tip in holotype.
In the pre-pharyngeal region, very abundant rhabditogen gland cells pierce the dorsal and marginal epidermis. These types of cells are scarce on the ventral epidermis; instead, there are gland cells producing erythrophil granules and scarce gland cells secreting cyanophil granules. There is no glandular margin (Fig.
The cutaneous musculature of the pre-pharyngeal region consists of a subepithelial circular muscle, followed by a diagonal layer with decussate fibers, and a longitudinal muscle organized in bundles (Fig.
The cutaneous and parenchymal musculature is organized in the cephalic region as in Ch. iheringi. A portion of the retractor muscle of the head is delta-shaped in a cross-section and ranges between 2–5 mm (or 5–14% of body length) from behind, 1–1.3 mm (2–3%) of the anterior extremity of the body (Fig.
The mouth is located in the middle of the pharyngeal pouch (n = 3) (Fig.
The testes are mature and dorsally located under the supra-intestinal transverse muscle layer, mostly placed between the intestinal diverticula. They extend from 12.7 mm (30% of body length, holotype) of the anterior extremity of the body to 0.5 mm before the root of the pharynx. Sperm ducts run immediately above the subintestinal parechymatic muscle layer. The sperm ducts bend dorsally close to the copulatory apparatus, and subsequently penetrate the ventral proximal region of the common muscle coat to open into the respective dilated branch of the prostatic vesicle (Fig.
Choeradoplana riutortae Lago-Barcia & Carbayo, sp. nov., holotype. Photomicrographs of sagittal sections A pharynx B prostatic vesicle. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
The male atrium is lined by a cuboidal, non-ciliated epithelium, and underlain by a 45–80 µm-thick layer of circular muscle with numerous interspersed longitudinal fibers (n = 3). The proximal half of the atrium receives two types of gland cells, one producing erythrophil granules, and a second type of scarce gland cells producing xanthophil granules; the distal half of the male atrium receives abundant gland cells producing xanthophil granules and the sub-apical portion of the cells of the lining epithelium contains xanthophil granules. The extrabulbar portion of the prostatic vesicle is coated by additional muscle fibers attaching it to the common muscle coat (Figs
Choeradoplana riutortae Lago-Barcia & Carbayo, sp. nov., holotype A photomicrograph of a sagittal section of the copulatory apparatus C Diagrammatic representation of the copulatory apparatus. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
The ovaries are mature, ovoid, 190 μm in length, and placed above the ventral nerve plate, and at a distance from the anterior body tip equal to 27% of body length (11.5 mm from anterior tip) (holotype). Ovovitelline ducts emerge from the dorso-lateral aspect of the ovaries and run above the ventral nerve plate. Lateral to the female atrium, the ovovitelline ducts bend medially and dorsally, then unite above the postero-dorsal section of the female atrium (Figs
Choeradoplana riutortae Lago-Barcia & Carbayo, sp. nov. Photomicrographs of sagittal sections A copulatory apparatus of paratype F4217 B copulatory apparatus of paratype F4261. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.
The female atrium is divided into a dilated canal running ventro-anteriorly and outside the common muscle coat, and a distal, funnel-shaped half is widely communicated with the male atrium (Figs
The common muscle coat is a very dense layer composed by densely packed muscle fibers variously oriented (Figs
Choeradoplana riutortae Lago-Barcia & Carbayo, sp. nov. matches all diagnostic characteristics of Choeradoplana. The external dorsal coloration resembles 11 species inside the genus with the background color being brownish with dark black or dark brown spots over it, namely Choeradoplana abaiba, Ch. agua, Ch. banga, Ch. benyai, Ch. bocaina, Ch. cyanoatria, Ch. longivesicula, Ch. pucupucu, and the herein described Ch. onae Lago-Barcia & Carbayo, sp. nov., Ch. eudoxiae Silva & Carbayo, sp. nov. and Ch. claudioi Lago-Barcia & Carbayo, sp. nov. However, none of them present the prominent cushions found in this species, nor the conspicuous red-orange coloration of the cephalic region.
With respect to the internal morphology, Ch. riutortae Lago-Barcia & Carbayo, sp. nov. is only similar to Ch. onae Lago-Barcia & Carbayo, sp. nov., Ch. bocaina and Ch. claudioi Lago-Barcia & Carbayo, sp. nov. in that the extrabulbar section of the prostatic vesicle is dish-shaped. However, the female atrium in Ch. claudioi Lago-Barcia & Carbayo, sp. nov. is partially below the male one (vs. behind, in Ch. riutortae Lago-Barcia & Carbayo, sp. nov.), whereas the male atrium in Ch. onae Lago-Barcia & Carbayo, sp. nov. has the same height along its length, (vs. a proximal, narrow half, and a distal, widened half). Finally, the male atrium in Ch. bocaina is 3× as long as the female, whereas this ratio is 1.2 in Ch. riutortae Lago-Barcia & Carbayo, sp. nov.
The monophyletic origin of the genus Choeradoplana was first demonstrated by
Choeradoplana is one among the few geoplanid genera which can be recognized through the body shape. The cephalic region in this genus is typically rolled up and the ventral surface of it is provided with glandular cushions, separated by a longitudinal groove. However, as shown above, the cephalic region of Ch. albonigra and Ch. eudoxiae Silva & Carbayo, sp. nov. lack the glandular cushions and it is not expanded laterally. In this respect, these two species cannot be distinguished from Cephaloflexa. Moreover, the anterior third of the body in Ch. albonigra narrows very gradually as in Cephaloflexa. Therefore, assignment to a genus must be based on internal aspects of these two species.
Another interesting observation is the distribution of the sensory pits. Following the diagnosis of Choeradoplana, these pits occur along a variable portion of the anterior region of the body, but they are absent in the apex (a feature also shared with Cephaloflexa). However, sensory pits in Ch. riutortae Lago-Barcia & Carbayo, sp. nov. contour the anterior extremity in one of the two examined specimens. Since the sensory pits in the apex are not present in all specimens, it can be interpreted as a deviant individual situation.
The diagnosis of Choeradoplana was emended by
Geoplaninae of elongated subcylindrical body. The cephalic region is kept rolled up and backwards; this region usually presents two glandular cushions, ventrally separated by a longitudinal groove. The cephalic region may be laterally dilated giving rise to a “neck” which differentiates this region from the remaining body. Eyes absent in the apex. Sensory pits absent in the apex. Broad creeping sole, more than one-third of body width. Strong cutaneous longitudinal muscles partially sunken into the parenchyma, exclusively ventrally or, more rarely, ventrally and dorsally too. Anteriorly all sunken ventral longitudinal fibers are medially concentrated, constituting the retractor unroller of the cephalic extremity. Bodies of rhabditogen cells located between the retractor and the epidermis. Common glandular ovovitelline duct approaching female genital canal dorsally from anterior direction, more rarely approaching behind the female atrium from the ventral direction.
Four of the six species studied in this paper (not Ch. albonigra and Ch. eudoxiae Silva & Carbayo, sp. nov.) present the external and internal characteristics of the genus Choeradoplana. The morphological diagnostic characteristics of this genus are remarkably heterogeneous in attributes found to be stable within other geoplanin genera. In addition to the variable shape of the cephalic region (discussed above), the longitudinal dorsal cutaneous musculature in Choeradoplana can be sunken (Ch. gladismariae Carbayo & Froehlich, 2012), a penis papilla can be present (Ch. crassiphalla, Ch. benyai, Ch. marthae), an inverted penis may also occur (Ch. minima Lemos & Leal-Zanchet, 2014), the prostatic vesicle may be intrabulbar (several species), the female genital canal can approach the female atrium behind it from the ventral direction (Ch. banga). Thus, we have increased the number of morphological variations seen in the genus in the present study, with the most remarkable being the ventral glandular cushions may be reduced or even absent, as in Ch. albonigra and Ch. eudoxiae Silva & Carbayo, sp. nov. and the anterior third of the body may become progressively thinner towards the anterior tip, as in Ch. albonigra. Therefore, one cannot trust the shape of the cephalic region for assigning a species with the head rolled-up to a genus. Instead, histological sections should be examined.
Despite the great variability in the diagnostic features, the genus can still be diagnosed by the following two exclusive attributes among Geoplanids: muscle retractor of the cephalic region delta-shaped in the cross-section and bodies of rhabditogen cells piercing the cephalic ventral epidermis are located between the retractor and the epidermis.
Dieter Fiege (Museum der Senckenbergischen Naturforschenden Gesellschaft in Frankfurt, Germany) kindly sent the holotype of C. albonigra on loan. ICMBio provided permit #11748-4 for the fieldwork. Ana Cristina Vasconcellos, Lucas Beltrami, and Geison Castro helped with histological sections. Marcus R. Hara and Fernando Portella de Luna Marques for their constructive comments on a previous version of the manuscript. Ana Laura Almeida is fully thanked for her help with molecular bench work. Ana María Rodríguez (University Carlos III de Madrid) is thanked for her help with the etymology, and Christopher Quinn for revision of the English text. DL-B thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq (Proc. 152971/2016-5) for a PhD fellowship. São Paulo Research Foundation (FAPESP, Process # 2019/12357-7) provided financial support to FC. Ana Maria Leal-Zanchet and Hugh Jones are gratefully acknowledged for their revision of the manuscript.